S Rule Body Size Clines in Passerines Along Tropical

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S Rule Body Size Clines in Passerines Along Tropical Journal of Biogeography (J. Biogeogr.) (2016) ORIGINAL Little evidence for Bergmann’s rule body ARTICLE size clines in passerines along tropical elevational gradients Benjamin G. Freeman1,2* 1Department of Ecology and Evolutionary ABSTRACT Biology, Cornell University, W257 Corson Aim To test whether intra- and interspecific patterns in body mass along Hall, Ithaca, NY, USA, 2Cornell Lab of elevational gradients follow Bergmann’s rule for a subset of tropical montane Ornithology, 159 Sapsucker Woods Rd, Ithaca, NY, USA passerines. Location Tropical elevational gradients in New Guinea, Borneo, Peru and Costa Rica. Methods I used linear regressions to assess intraspecific patterns in body mass along elevational gradients in common New Guinean passerines (2697 mist- netted individuals of 21 species). I then evaluated interspecific patterns using two data sets. First, I investigated differences in body mass in species pairs of elevational replacements, closely related species with minimal overlap along elevational gradients (species pairs; New Guinea: n = 45, Borneo: n = 22, Peru: n = 58 and Costa Rica: n = 30). Second, I used a comparative phylogenetic approach to test whether species’ mid-point elevations predicted their masses within entire passerine avifaunas found along single elevational gradients (species; New Guinea: n = 184, Peru: n = 529 and Costa Rica: n = 220). Results New Guinean passerines exhibited minimal intraspecific variation in mass along elevational gradients. In two species, lower elevation individuals had significantly larger masses than upper elevation conspecifics. In species pairs of elevational replacements, there was no trend for upper elevation species to have larger masses than lower elevation species. Overall, species pairs tended to have positive mass disparities (mass of upper elevation species/mass of lower elevation species). However, contrary to predictions of Bergmann’s rule, mass disparity was unrelated to elevational overlap. When considering entire passerine avifaunas along single elevational gradients, species’ masses were uncorrelated with their mid-point elevational distributions. Main conclusions I found little evidence that tropical montane passerines have larger body masses at higher elevations where temperatures are colder. This lack of pattern was consistent across evolutionarily independent avifaunas of different biogeographical regions. These results suggest mean temperature is not a gener- ally important driver of body size evolution in tropical montane passerines. *Correspondence: Benjamin G. Freeman, Department of Ecology and Evolutionary Keywords Biology, Cornell University, W257 Corson Bergmann’s rule, body size, body size clines, comparative phylogenetics, Hall, Ithaca, NY, USA. E-mail: [email protected] ecogeographic rule, elevational gradient, tropical mountains drive the evolution of body size (Brown et al., 2004), tem- INTRODUCTION perature is one potentially important abiotic factor influenc- Body size is an ecologically influential trait that varies widely ing body size evolution – Bergmann’s rule describes the within and among species (LaBarbera, 1989; Brown et al., pattern that populations or species of endotherms living in 2004). Although many abiotic and biotic mechanisms can colder environments tend to be larger than related ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12812 B. G. Freeman populations or species living in warmer environments elevations as predicted by Bergmann’s rule. I addressed this (Bergmann, 1847; James, 1970). The proper formulation of question by testing how body sizes in the largest group of Bergmann’s rule remains debated; perhaps most importantly, tropical montane birds – the passerines – are related to their Bergmann’s rule has been considered both a pattern (a nega- elevational distributions. To assess the generality of any pat- tive relationship between body size and temperature) and a terns (or lack thereof), I investigate the relationship between process (temperature exerts selection on body size via physio- body mass and elevational distribution in interspecific com- logical mechanisms such as thermoregulation; e.g. Watt et al., parisons within the evolutionarily distinct avifaunas of the 2010; Meiri, 2011; Olalla-Tarraga, 2011; Watt & Salewski, Neotropics, Southeast Asia and Melanesia. I consider Berg- 2011). Investigations of Bergmann’s rule have traditionally mann’s rule to simply be a negative relationship between analysed body size clines along latitudinal gradients (e.g. body size and temperature (i.e. a pattern; hereafter ‘Berg- Ashton, 2002; Ashton & Feldman, 2003; Watt et al., 2010; mann’s rule’). As such, Bergmann’s rule predicts that (1) Feldman & Meiri, 2014). However, temperature declines not within species, individuals at high elevations should tend to only with increasing latitude, but also with increasing eleva- be larger than individuals at low elevations, (2) within spe- tion; thus, studies have also analysed whether Bergmann’s cies pairs of closely related species, upper elevation species rule patterns are found in body size clines along elevational should be larger than lower elevation species, with this rela- gradients (e.g. Brehm & Fiedler, 2004; Herzog et al., 2013). tionship strongest in species pairs that inhabit non-overlap- Tropical elevational gradients offer an excellent geographi- ping elevational distributions (and thus experience more cal arena to investigate whether body size clines are associ- different ambient temperatures relative to species pairs with ated with temperature. Temperatures decline over short greater elevational overlap) and (3) when accounting for distances along tropical mountain slopes, where ambient phylogenetic relationships, elevational distributions should be mean temperature drops c. 5–6 °C per 1000 m gain in eleva- significantly positively related to body size in large assem- tion (Forero-Medina et al., 2011; Freeman & Class Freeman, blages of species. I tested these predictions using (1) field 2014a). As a consequence, sites on steep slopes may be data for common species of New Guinean understorey located just a few kilometres apart but experience very differ- passerines captured along two single elevational gradients, ent temperatures. Because temperature variation is typically (2) relative body masses in species pairs of closely related minimal at particular sites along tropical elevational gradi- species that inhabit minimally overlapping elevational distri- ents (e.g. daily temperatures at a given site within the forest butions along an elevational gradient in four distinct tropical understorey vary by c. 5 °C, and annual variation is typically montane regions (the Eastern highlands of New Guinea, minor), sedentary tropical organisms separated by even small Manu National Park in the Peruvian Andes, the Caribbean (c. 750 m) expanses of elevation can experience completely slope of Costa Rica and the highlands of Malaysian Borneo) distinct temperatures, at least in the shaded forest interior and (3) phylogenetic comparative methods to assess whether (Janzen, 1967). species’ mid-point elevational distributions significantly pre- Evidence that tropical and subtropical montane faunas dicts their body size in the entire passerine avifaunas found exhibit body size clines consistent with Bergmann’s rule in three regions (the Eastern highlands of New Guinea, along elevational gradients is mixed. Increases in body size in Manu National Park in the Peruvian Andes and the Carib- colder high elevation environments within species have been bean slope of Costa Rica). Taken together, these analyses found in some cases (e.g. Rand, 1936; Lu et al., 2006; Van- provide a general test of whether tropical montane passerines derwerf, 2012), and in interspecific comparisons in clades of conform to Bergmann’s rule. Neotropical frogs (Gouveia et al., 2013) and lizards (Cruz et al., 2005; Zamora-Camacho et al., 2014), but not in clades MATERIALS AND METHODS of Asian frogs (Hu et al., 2011) or Neotropical butterflies (Hawkins & Devries, 1996), moths (Brehm & Fiedler, 2004) Intraspecific or dung beetles (Herzog et al., 2013). Results can be incon- sistent within a taxonomic group in a single geographical Bergmann’s rule predicts that, within species, individuals region. For example, patterns of intraspecific body size varia- should tend to have larger masses at high elevations. I tested tion in Andean birds follow Bergmann’s rule in some (Tray- this prediction using field body mass data gathered along lor, 1950; Graves, 1991; Bulgarella et al., 2007) but not all two elevational gradients in Papua New Guinea: the YUS (Remsen, 1984, 1993) species, including an example where a Conservation Area, Morobe Province and the north-west species exhibits Bergmann’s rule body size clines across lati- ridge of Mt Karimui, Chimbu Province. The YUS Conserva- tudinal but not elevational gradients (Gutierrez-Pinto et al., tion Area (hereafter YUS, approximate coordinates: À6.00, 2014). This inconsistency holds for analyses at the interspeci- 146.84) is located on the northern scarp of the Saruwaged fic level – some clades of tropical birds exhibit Bergmann’s Range on the Huon Peninsula. Between 2010 and 2012, a rule body size clines while others do not (Blackburn & Rug- team of fieldworkers conducted mist-net surveys in primary giero, 2001). forest along a single elevational gradient from 230 to 2940 m Thus, it remains unclear whether tropical montane birds in YUS; a total of 18 mist-net
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